Microorganisms are essential components of underground life systems and drive elemental cycling between plants and soil. Yet, in the ecologically fragile Loess Plateau, scant attention has been paid to the response of microbial communities to organic carbon (C) chemistry of both leaves and soils under different revegetation conditions, as well as subsequent alternation in their C metabolic functions. Here, Fourier transform infrared (FTIR) spectrum, amplicon sequencing of 16S rRNA and ITS, and temporal incubation with Biolog-Eco 96 plates were combined to explore the vegetative heterogeneity of microbial community properties and metabolic functions, as well as their regulatory mechanisms in three typical revegetation types including Robinia pseudoacacia L. (RF), Caragana korshinskii KOM. (SL), and abandoned grassland (AG). We observed higher bacterial-to-fungal ratios (B: F = 270.18) and richer copiotrophic bacteria (Proteobacteria = 33.08%) in RF soil than those in AG soil, suggesting that microbes were dominated by r-strategists in soil under RF treatment, which is mainly related to long-term priming of highly bioavailable leaf C (higher proportion of aromatic and hydrophilic functional groups and lower hydrophobicity). Conversely, microbial taxa in AG soil, which was characterized by higher leaf organic C hydrophobicity (1.39), were dominated by relatively more abundant fungi (lower B: F ratio = 149.49) and oligotrophic bacteria (Actinobacteria = 29.30%). The co-occurrence network analysis showed that microbial interactive associations in RF and AG soil were more complex and connective than in SL soil. Furthermore, Biolog-Eco plate experiments revealed that microorganisms tended to utilize labile C compounds (carbohydrates and amino acids) in RF soil and resistant C compounds (polymers) in AG soil, which were consistent with the substrate adaptation strategies of predominant microbial trophic groups in different revegetation environments. Meanwhile, we observed greater microbial metabolic activity and diversity advantages in RF vegetation. Collectively, we suggest that besides the nutrient variables in the leaf-soil system, the long-term regulation of the microbial community by the C chemistry of the leaf sequentially alters the microbial metabolic profiles in a domino-like manner. RF afforestation is more conducive to restoring soil microbial fertility (including microbial abundance, diversity, interactive association, and metabolic capacity). Our study potentially paves the way for achieving well-managed soil health and accurate prediction of C pool dynamics in areas undergoing ecological restoration of the Loess Plateau.
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